Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep
Abstract Motor skills dynamically evolve during practice and after training. Using magnetoencephalography, we investigated the neural dynamics underpinning motor learning and its consolidation in relation to sleep during resting-state periods after the end of learning (boost window, within 30 min) a...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-03-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-024-58123-6 |
| _version_ | 1827301245923098624 |
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| author | Liliia Roshchupkina Vincent Wens Nicolas Coquelet Charline Urbain Xavier de Tiege Philippe Peigneux |
| author_facet | Liliia Roshchupkina Vincent Wens Nicolas Coquelet Charline Urbain Xavier de Tiege Philippe Peigneux |
| author_sort | Liliia Roshchupkina |
| collection | DOAJ |
| description | Abstract Motor skills dynamically evolve during practice and after training. Using magnetoencephalography, we investigated the neural dynamics underpinning motor learning and its consolidation in relation to sleep during resting-state periods after the end of learning (boost window, within 30 min) and at delayed time scales (silent 4 h and next day 24 h windows) with intermediate daytime sleep or wakefulness. Resting-state neural dynamics were investigated at fast (sub-second) and slower (supra-second) timescales using Hidden Markov modelling (HMM) and functional connectivity (FC), respectively, and their relationship to motor performance. HMM results show that fast dynamic activities in a Temporal/Sensorimotor state network predict individual motor performance, suggesting a trait-like association between rapidly recurrent neural patterns and motor behaviour. Short, post-training task re-exposure modulated neural network characteristics during the boost but not the silent window. Re-exposure-related induction effects were observed on the next day, to a lesser extent than during the boost window. Daytime naps did not modulate memory consolidation at the behavioural and neural levels. These results emphasise the critical role of the transient boost window in motor learning and memory consolidation and provide further insights into the relationship between the multiscale neural dynamics of brain networks, motor learning, and consolidation. |
| first_indexed | 2024-04-24T16:19:42Z |
| format | Article |
| id | doaj.art-5ee251ff7ae041dbb066f7761d4f0c35 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-24T16:19:42Z |
| publishDate | 2024-03-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-5ee251ff7ae041dbb066f7761d4f0c352024-03-31T11:16:18ZengNature PortfolioScientific Reports2045-23222024-03-0114111810.1038/s41598-024-58123-6Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleepLiliia Roshchupkina0Vincent Wens1Nicolas Coquelet2Charline Urbain3Xavier de Tiege4Philippe Peigneux5UR2NF - Neuropsychology and Functional Neuroimaging Research Unit Affiliated at CRCN - Centre for Research in Cognition and Neurosciences, Université Libre de Bruxelles (ULB)UNI - ULB Neuroscience InstituteUNI - ULB Neuroscience InstituteUR2NF - Neuropsychology and Functional Neuroimaging Research Unit Affiliated at CRCN - Centre for Research in Cognition and Neurosciences, Université Libre de Bruxelles (ULB)UNI - ULB Neuroscience InstituteUR2NF - Neuropsychology and Functional Neuroimaging Research Unit Affiliated at CRCN - Centre for Research in Cognition and Neurosciences, Université Libre de Bruxelles (ULB)Abstract Motor skills dynamically evolve during practice and after training. Using magnetoencephalography, we investigated the neural dynamics underpinning motor learning and its consolidation in relation to sleep during resting-state periods after the end of learning (boost window, within 30 min) and at delayed time scales (silent 4 h and next day 24 h windows) with intermediate daytime sleep or wakefulness. Resting-state neural dynamics were investigated at fast (sub-second) and slower (supra-second) timescales using Hidden Markov modelling (HMM) and functional connectivity (FC), respectively, and their relationship to motor performance. HMM results show that fast dynamic activities in a Temporal/Sensorimotor state network predict individual motor performance, suggesting a trait-like association between rapidly recurrent neural patterns and motor behaviour. Short, post-training task re-exposure modulated neural network characteristics during the boost but not the silent window. Re-exposure-related induction effects were observed on the next day, to a lesser extent than during the boost window. Daytime naps did not modulate memory consolidation at the behavioural and neural levels. These results emphasise the critical role of the transient boost window in motor learning and memory consolidation and provide further insights into the relationship between the multiscale neural dynamics of brain networks, motor learning, and consolidation.https://doi.org/10.1038/s41598-024-58123-6 |
| spellingShingle | Liliia Roshchupkina Vincent Wens Nicolas Coquelet Charline Urbain Xavier de Tiege Philippe Peigneux Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep Scientific Reports |
| title | Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep |
| title_full | Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep |
| title_fullStr | Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep |
| title_full_unstemmed | Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep |
| title_short | Motor learning- and consolidation-related resting state fast and slow brain dynamics across wake and sleep |
| title_sort | motor learning and consolidation related resting state fast and slow brain dynamics across wake and sleep |
| url | https://doi.org/10.1038/s41598-024-58123-6 |
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